Abstract

Aggression is an evolutionarily conserved behavior across the animal kingdom. Aggressive behavior among conspecifics is critical for the acquisition and defense of important resources including food, mates, and shelter, hence contributing to the survival and reproduction of animals. Therefore, it is of particular interest to understand how this behavior is regulated.
We use the fruit fly Drosophila melanogaster as a model system to understand the regulation of aggression. We identify Cyp6a20, a cytochrome P450, as a gene mediating the suppressive effect of social experience on the intensity of male-male aggression. Notably, Cyp6a20 has been previously identified by profiling Drosophila strains subjected to genetic selection for differences in aggressiveness. Therefore our findings reveal a common genetic target for environmental and heritable influences on aggressiveness. Interestingly, Cyp6a20 is expressed in a subset of non-neuronal support cells associated with pheromone-sensing olfactory sensilla, suggesting that olfactory pheromone(s) may contribute to the regulation of aggression. Consistent with this idea, we find that cis-11-vaccenyl acetate (cVA), a previously identified olfactory pheromone, promotes male-male aggression via a group of olfactory receptor neurons expressing Or67d.
Despite its robust behavioral effect, cVA is not required for baseline male-male aggression, and exogenous cVA does not induce male-female aggression, suggesting that sex specificity of male aggression is independent of cVA. Our subsequent studies show that the sex specificity of male social behaviors is determined by a different class of pheromones, named male cuticular hydrocarbons. Male flies perform significantly less aggression and more courtship towards male flies lacking male CHs, both of which can be rescued by synthetic (Z)-7-tricosene (7-T), the most abundant male cuticular hydrocarbon. The opposite influences of 7-T on aggression and courtship are independent, but both require the gustatory receptor Gr32a. Surprisingly, sensitivity to 7-T is required for the aggression-promoting effect of cVA, but not vice versa. Furthermore, the increased courtship in the absence of male cuticular hydrocarbons is induced by pheromone(s) detected by an olfactory receptor Or47b. Thus, male social behaviors are controlled by gustatory pheromones that promote and suppress aggression and courtship, respectively, and whose influences are dominant to olfactory pheromones that enhance these behaviors.